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Complete genome sequence of Pseudoalteromonas phage vB_PspS-H40/1 (formerly H40/1) that infects Pseudoalteromonas sp. strain H40 and is used as biological tracer in hydrological transport studies

  • René Kallies1Email authorView ORCID ID profile,
  • Bärbel Kiesel1,
  • Matthias Schmidt2,
  • Johannes Kacza3,
  • Nawras Ghanem1,
  • Anja Narr1,
  • Jakob Zopfi4,
  • Lukas Y. Wick1,
  • Jörg Hackermüller5,
  • Hauke Harms1, 6 and
  • Antonis Chatzinotas1, 6
Standards in Genomic Sciences201712:20

Received: 18 June 2016

Accepted: 22 January 2017

Published: 2 February 2017


Pseudoalteromonas phage vB_PspS-H40/1 is a lytic phage that infects Pseudoalteromonas sp. strain H40. Both, the phage and its host were isolated in the 1970s from seawater samples collected from the North Sea near the island of Helgoland, Germany. The phage particle has an icosahedral capsid with a diameter of ~43 to 45 nm and a long non-contractile tail of ~68 nm in length, a typical morphology for members of the Siphoviridae family. The linear dsDNA genome of Pseudoalteromonas phage vB_PspS-H40/1 has a sequence length of 45,306 bp and a GC content of 40.6%. The genome has a modular structure and contains a high proportion of sequence information for hypothetical proteins, typically seen in phage genome sequences. This is the first report of the complete genome sequence of this lytic phage, which has been frequently used since the 1990s as biological tracer in hydrogeological transport studies.


Pseudoalteromonas phage Siphoviridae AquaDivaMarine phageVirusGenomeBacteriophages as tracers


Pseudoalteromonas , affiliated with the order Alteromonadales [1, 2] of the Gammaproteobacteria [2, 3], is a genus of heterotrophic, Gram-negative marine bacteria [4]. Members of this genus are widely distributed in marine ecosystems and have attracted interest due to their frequent association with eukaryotic hosts and their production of biologically active compounds [57]. Both inhibitory as well as synergistic chemical interactions between strains of Pseudoalteromonas and various marine eukaryotes have been described [8], indicating that members of this genus are potentially involved in complex ecological networks across trophic levels. Viruses, as the most abundant biological entity in the oceans, are a major cause of host mortality and thus key players within these ecological networks; they influence host community structures and thereby also influence global biogeochemical cycles and genetic landscapes [9].

As of April 2016, 14 complete Pseudoalteromonas phage genomes have been deposited at GenBank (10 of them unpublished). Ten representatives belong to the Caudovirales order (three siphoviruses, four podoviruses, two myoviruses and one unclassified caudovirus), one is a corticovirus and three are unclassified viruses. Pseudoalteromonas phages have been shown to represent a significant group of phages in the ocean [10, 11], making it likely that the number of yet unknown phage genomes is much higher. Characterization of additional Pseudoalteromonas phage genomes is a further step towards a better understanding of the diversity, the biology and the ecological impact of this group of phages and contributes to an improved interpretation of viral metagenome data and dynamics of viral populations in the environment [1214]. Moreover, comparison of potentially closely related viral genomes is a prerequisite to understand virus evolution and intraspecies genomic variation [15, 16].

In this report we describe the genome of the Pseudoalteromonas phage vB_PspS-H40/1, isolated in 1978 from the North Sea near the island of Helgoland (Germany) [17]. Notably, this phage has been used as a non-reactive biological agent to trace the flow of water in surface and subsurface environments and promises utility in (geo-)hydrological transport studies [1821]. According to the scheme for the nomenclature of viruses the phage was re-named from H40/1 to vB_PspS-H40/1 [22].

Organism Information

Classification and features

The bacterial host H40 was isolated from seawater samples collected between 1969 and 1978 near the island of Helgoland in the North Sea [17]. Sequence analysis of the 16S-rRNA gene revealed H40 as a member of the Pseudoalteromonas genus. The partial 16S-rRNA sequence was deposited at GenBank (acc. no. KX236488). Strain H40 was used as the bacterial host for screening of lytic marine bacteriophages from the same sampling site resulting in the isolation of phage vB_PspS-H40/1 [17].

Pseudoalteromonas phage vB_PspS-H40/1 is a lytic phage forming clear, well-contrasted plaques of four to five mm in diameter. Transmission electron microscopy showed that vB_PspS-H40/1 is a B1 morphotype with an icosahedral capsid of 42.7 nm in length (±1.7 nm) and 44.5 nm in width (± 2 nm). The long, non-contractile tail had a length of 67.5 nm (± 3.9 nm) and a diameter of 6.7 nm (± 0.6 nm) (Fig. 1). These morphological characteristics are typical for members belonging to the Siphoviridae family of the order Caudovirales [23].
Fig. 1

Transmission electron micrograph of Pseudoalteromonas phage vB_PspS-H40/1 infecting Pseudoalteromonas sp. strain H40. Virus particles were stained with 2% tungstophosphoric acid and visualized using an electron microscope Libra 120 (Zeiss, Oberkochen, Germany). Size bar: 40 nm

The phage surface is moderately charged (zeta potential of −11 ± 3 mV (100 mM K2HPO4/KH2PO4, pH = 7)) and of moderate hydrophobicity (water contact angle = 53 ± 3°) as determined by standard physico-chemical characterization methods of bacterial surfaces (e.g. [24]).

Pseudoalteromonas phage vB_PspS-H40/1 has a linear dsDNA genome comprising 45,306 bp with a GC content of 40.6%. It showed the highest similarity (55.3% identity) over the whole genome to Pseudoalteromonas phage H103 (GenBank acc. no. KP994596), an unclassified representative of the Caudovirales order infecting the marine host Pseudoalteromonas marina [25] (Fig. 2). Phylogenetic analysis of the terminase large subunit (TerL) amino acid sequence grouped phage vB_PspS-H40/1 together with phage H103 in one clade (Fig. 3). Both phages shared a most recent common ancestor with TerL sequences found in unclassified members of the Caudovirales order and (probably) prophage sequences from members of the bacterial family Enterobacteriaceae [26, 27]. These unclassified phages belong to all three families of the Caudovirales order, i.e. Siphoviridae, Podoviridae and Myoviridae. Taken together, TerL-based phylogenetic analysis indicates phage vB_PspS-H40/1 occupies (perhaps together with phage H103) a phylogenetic position distinct from established genera of the Siphoviridae family.
Fig. 2

Genome maps of Pseudoalteromonas phages vB_PspS-H40/1 and H103. Protein coding sequences are presented by arrows and their functions are indicated by colours: red, DNA packaging; green, structural genes, blue, DNA replication and metabolism; grey, hypothetical proteins. Similarities between both genomes were calculated using tblastx [36]. Similarities are shown in blue according to the scale on the left side. The figure was drawn using Easyfig [44]

Fig. 3

Maximum-likelihood phylogenetic tree based on the TerL amino acid sequences indicating the phylogenetic relationship of Pseudoalteromonas phage vB_PspS-H40/1 (shown in blue) to related phages and bacterial sequences (probably prophages). Analyses were performed guided by the Jones-Taylor-Thornton substitution model using PhyML [45]. Confidence testing was performed by 500 bootstrap replicates. Bootstrap values are shown next to the nodes. GenBank accession numbers and genera are shown in parentheses. Bar represents 0.7 substitution per amino acid position

Phylogenetic classification and general features of Pseudoalteromonas phage vB_PspS-H40/1 are summarized in Table 1.
Table 1

Classification and general features of Pseudoalteromonas phage vB_PspS-H40/1 infecting Pseudoalteromonas sp. strain H40




Evidence codea



Domain: N/A


Genome group: dsDNA viruses, no RNA stage



Phylum: unassigned


Class: unassigned


Order: Caudovirales

TAS [23]


Family: Siphoviridae

TAS [23]


Genus: unassigned


Species: unassigned


Strain: vB_PspS-H40/1


Particle shape

Isometric capsid, long non-contractile tail



Gram strain



Cell shape









Temperature range



Optimum temperature



pH range; optimum



Carbon source





Marine water column

TAS [17]






Oxygen requirement




Biotic relationship

Intracellular parasite of Pseudoalteromonas sp. strain H40

TAS [17]



Virulent phage of Pseudoalteromonas sp. strain H40



Geographic location

North Sea, Helgoland, Germany

TAS [17]


Sample collection


TAS [17]













aEvidence codes - IDA inferred from direct assay, TAS traceable author statement, N/A not applicable. These evidence codes are from the Gene Ontology project [46]

Genome sequencing information

Genome project history

Pseudoalteromonas phage vB_PspS-H40/1 is one of the few known marine siphovirus isolates [28] and belongs to a group of important phages found in the ocean [10, 11]. Genome sequencing of this phage will increase available information and facilitate future studies on diversity, evolution and ecological impact of marine viruses. A second reason to select this phage for sequencing is its frequent application in biological tracing experiments [1821]. Phage vB_PspS-H40/1 is one of the marine phages that are currently used in the frame of the Collaborative Research Centre AquaDiva to trace the hydrological flow and reactive transport of colloidal particles from the surface into the Earth’s subsurface [29]. Environmental influences might inactivate a still to define percentage of transported phages. Knowledge of a phage genome will facilitate the detection of this phage using PCR and thus allow to (quantitatively) distinguish between biologically active (e.g. detected by plaque assay) from inactive phages and might hence help in the interpretation of findings from these transport experiments.

The dsDNA genome of phage vB_PspS-H40/1 was sequenced using the Illumina MiSeq system. Experiments, genome assembly, annotation and submission to GenBank were performed at the Department of Environmental Microbiology at the Helmholtz Centre for Environmental Research - UFZ, Leipzig, Germany. The sequencing project was started in December 2015 and finished in February 2016 and its outcome is available in the Genome Online Database under project number Gp0133998. The complete annotated genome sequence was submitted to Genbank (GenBank acc. no. KU747973). Information on the project is summarized in Table 2.
Table 2

Project information





Finishing quality



Libraries used

One paired-end Illumina library


Sequencing platforms

Illumina MiSeq

MIGS 31.2

Fold coverage




Geneious Assembler version R6


Gene calling method

RAST, GLIMMER, GeneMark.hmm


Locus Tag



Genbank ID



GenBank Date of Release

Jun 07, 2016








Source Material Identifier



Project relevance

Diversity of marine bacteriophage, Hydrological transport studies

a NA not available

Growth conditions and genomic DNA preparation

The bacterial host Pseudoalteromonas sp., strain H40 was grown and maintained in 2216E medium [30] (containing nutrients at 50% of the original concentration) at 20 °C. The phage was propagated on its host in petri dishes with 2216E agar (with nutrients as above) using the double agar-layer technique. Five ml of SM buffer (100 mM NaCl, 8 mM MgSO4 × 7H2O, 50 mM Tris–HCl, pH 7.5) and a few drops of chloroform were added to the plates after confluent lysis of bacterial host cells. Plates were gently shaken for 2 h at room temperature, supernatant was collected and cell debris was removed by centrifugation at 10,000 × g for 15 min. One volume of chloroform was then added to the supernatant, gently mixed and centrifuged at 5,000 × g for 5 min. The phage particle-containing upper phase was passed through a 0.22 μm polyvinylidene fluoride CHROMAFIL® membrane filter to remove unlysed host cells and debris. The resulting phage suspension was stored at 4 °C. DNA from phage particles was extracted following the protocol of Thurber et al. [31].

Genome sequencing and assembly

The extracted phage DNA was sheared into ~300 to 500 bp fragments using the Covaris M220 Focused-ultrasonicator™ instrument and one paired-end library was prepared with the NEBNext® Ultra™ DNA Library Prep Kit for Illumina®. Sequencing was performed at the Helmholtz Centre for Environmental Research - UFZ on an Illumina MiSeq system (2 × 150 bp). In total, 418,468 paired-reads were obtained for Pseudoalteromonas phage vB_PspS-H40/1. Raw reads were split into 10 subsets (approximately 42,000 reads for each subset) to facilitate improved assembly [32]. Independent assemblies were performed for each subset by Geneious Assembler (version R6) resulting in nearly the same single contig for each of the subsets but with different starting points indicating a circularly permuted genome of phage vB_PspS-H40/1. For confirmation, PCR primers were designed matching the ends of the contigs with an outward orientation and used in PCR. The resulting amplicon was Sanger sequenced and used to close the contigs for Pseudoalteromonas phage vB_PspS-H40/1. The coverage was estimated by reference mapping of the raw reads to the contig resulting in an approximate 1200-fold coverage (~ 92% of all reads) of the 45,306 bp genome.

Genome annotation

Genes and ORFs in the phage genome were predicted using a combination of three gene calling methods: the RAST annotation server [33], GLIMMER3 [34] and GeneMark.hmm [35]. Only ORFs that were predicted by two of the three gene calling methods were included in the annotation. Functional annotation of translated ORFs was improved by BLASTp alignments against the NCBI non-redundant database [36]. In addition, RPS-BLAST searches against the Conserved Domain Database [37] and HMMER search [38] against the UniProtKB database were performed. Protein domains were predicted using the COG [39], Pfam [40], TIGRFAMs [41] and KEGG [42] databases. Phoebius [43] was used to predict signal peptides and transmembrane helices.

Genome properties

The complete genome of Pseudoalteromonas phage vB_PspS-H40/1 was assembled into one linear contig of 45,306 bp with a GC content of 40.6%. In total, 73 putative coding sequences were predicted in the phage genome (Fig. 2, Additional file 1: Table S1). Seventeen of these 73 protein coding genes were assigned to putative protein functions. The functions of the remaining 56 putative protein coding genes remained unknown and they were annotated as hypothetical proteins. One gene with a signal peptide was identified together with eight proteins containing transmembrane helices. Pseudoalteromonas phage vB_PspS-H40/1 genome properties are summarized in Table 3 and genes assigned to COG functional categories are listed in Table 4.
Table 3

Genome statistics



% of Total

Genome size (bp)



DNA coding (bp)



DNA G + C (bp)



DNA scaffolds



Total genes



Protein coding genes



RNA genes



Pseudo genes



Genes in internal clusters



Genes with function prediction



Genes assigned to COGs



Genes with Pfam domains



Genes with signal peptides



Genes with transmembrane helices



CRISPR repeats



Table 4

Number of genes associated with general COG functional categories








Translation, ribosomal structure and biogenesis




RNA processing and modification








Replication, recombination and repair




Chromatin structure and dynamics




Cell cycle control, Cell division, chromosome partitioning




Defense mechanisms




Signal transduction mechanisms




Cell wall/membrane biogenesis




Cell motility




Intracellular trafficking and secretion




Posttranslational modification, protein turnover, chaperones




Energy production and conversion




Carbohydrate transport and metabolism




Amino acid transport and metabolism




Nucleotide transport and metabolism




Coenzyme transport and metabolism




Lipid transport and metabolism




Inorganic ion transport and metabolism




Secondary metabolites biosynthesis, transport and catabolism




General function prediction only




Function unknown




Not in COGs

The total is based on the total number of protein coding genes in the genome

Insights from the genome sequence

When all 73 predicted CDSs were subjected to functional annotation only 17 CDSs could be assigned to a specific function. These functions were related to DNA packaging, head and tail assembly, DNA replication and metabolism (Fig. 2 and Additional file 1: Table S1). Twenty-nine of the predicted CDSs, including mainly hypothetical proteins but also TerL and structural proteins, showed highest similarity to the unclassified Caudovirales member Pseudoalteromonas phage H103 after blastp analysis (Fig. 2). Highest similarity of other CDSs was found to marine Pseudoalteromonas phages belonging to the Siphoviridae family, i.e. Pseudoalteromonas phage TW1 (GenBank acc. no. KC542353), Pseudoalteromonas phage Pq0 (GenBank acc. no. NC_029100) and Pseudoalteromonas phage H105/1 (GenBank acc. no. NC_015293). However, proteins involved in DNA replication (helicase, RecA-NTPase and methylase) were related to those found in Vibrio phage H188 (GenBank KT160311) and Escherichia phage vB_EcoM-ep3 (GenBank acc. no. NC_025430), two members of the Myoviridae family, suggesting mosaicism of the genome.

Phylogenetic inferences deduced from the TerL amino acid sequence showed no close phylogenetic relationship to any of the established Siphoviridae genera (Fig. 3).


The characterized complete genome of lytic Pseudoalteromonas phage vB_PspS-H40/1 that was isolated from seawater in the North Sea improves our knowledge of this significant group of phages. The linear dsDNA genome has a size of 45,306 bp and a GC content of 40.6%. The obtained sequencing data indicate phage vB_PspS-H40/1 uses headful packaging strategy and that the genome is circularly permuted. Among the 73 protein coding sequences only 17 were functionally annotated. Transmission electron microscopy and phylogenetic analysis of TerL sequences suggest this phage might belong to a genus of a yet unclassified group of Siphoviridae. Next to studies on specific phage-host interactions in marine systems, phage vB_PspS-H40/1 will be used in surface and groundwater tracer experiments and its genome sequence and morphological description will help interpreting results from these studies.



Terminase large subunit



We are grateful for excellent technical assistance of Stephan Schreiber and Nicole Steinbach.


The work has been funded by the Deutsche Forschungsgemeinschaft (DFG) CRC 1076 “AquaDiva”. The analytical facilities of ProVIS - Centre for Chemical Microscopy at the Helmholtz Centre for Environmental Research were supported by Europäischer Fonds für regionale Entwicklung (EFRE), Freistaat Sachsen and the Helmholtz Association.

Author’s contributions

RK, NG and AN performed laboratory experiments. RK analysed the data. BK, MS and JK performed electron microscopy. RK, JZ, LW, JH, HH and AC together designed the study and wrote the manuscript. All authors read and approved the final version of the manuscript.

Competing interests

The authors declare that they have no competing interests.

Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (, which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( applies to the data made available in this article, unless otherwise stated.

Authors’ Affiliations

Department of Environmental Microbiology, Helmholtz Centre for Environmental Research - UFZ, Leipzig, Germany
Department of Isotope Biogeochemistry, ProVis - Centre for Chemical Microscopy, Helmholtz Centre for Environmental Research - UFZ, Leipzig, Germany
Institute of Anatomy, Histology and Embryology, Faculty of Veterinary Medicine, University of Leipzig, Leipzig, Germany
Department of Environmental Sciences - Aquatic and Stable Isotope Biogeochemistry, University of Basel, Basel, Switzerland
Young Investigators Group Bioinformatics & Transcriptomics, Helmholtz Centre for Environmental Research - UFZ, Leipzig, Germany
German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig, Deutscher Platz 5e, Leipzig, Germany


  1. Bowman JP, McMeekin TA. Order X. Alteromonadales ord. nov. In: Brenner DJ, Krieg NR, Staley JT, Garrity GM, editors. Bergey’s Manual of Systematic Bacteriology, vol. 2. 2nd ed. New York: Springer; 2005. p. 443. The Proteobacteria), part B (The Gammaproteobacteria.View ArticleGoogle Scholar
  2. List Editor. Validation of publication of new names and new combinations previously effectively published outside the IJSEM. List no. 106. Int J Syst Evol Microbiol. 2005;55:2235.View ArticleGoogle Scholar
  3. Garrity GM, Bell JA, Lilburn T. Class III. Gammaproteobacteria class. nov. In: Brenner DJ, Krieg NR, Staley JT, Garrity GM, editors. Bergey’s Manual of Systematic Bacteriology, vol. 2. 2nd ed. New York: Springer; 2005. p. 1. The Proteobacteria), part B (The Gammaproteobacteria.View ArticleGoogle Scholar
  4. Gauthier G, Gauthier M, Christen R. Phylogenetic analysis of the genera Alteromonas, Shewanella, and Moritella using genes coding for small-subunit rRNA sequences and division of the genus Alteromonas into two genera, Alteromonas (emended) and Pseudoalteromonas gen. nov., and proposal of twelve new species combinations. Int J Syst Bacteriol. 1995;45:755–61.View ArticlePubMedGoogle Scholar
  5. Holmström C, Kjelleberg S. Marine Pseudoalteromonas species are associated with higher organisms and produce biologically active extracellular agents. FEMS Microbiol Ecol. 1999;30:285–93.View ArticlePubMedGoogle Scholar
  6. Skovhus TL, Ramsing NB, Holmström C, Kjelleberg S, Dahllöf I. Real-time quantitative PCR for assessment of abundance of Pseudoalteromonas species in marine samples. Appl Environ Microbiol. 2004;70:2373–82.View ArticlePubMedPubMed CentralGoogle Scholar
  7. Skovhus TL, Holmström C, Kjelleberg S, Dahllöf I. Molecular investigation of the distribution, abundance and diversity of the genus Pseudoalteromonas in marine samples. FEMS Microbiol Ecol. 2007;61(2):348–61.View ArticlePubMedGoogle Scholar
  8. Bowman JP. Bioactive compound synthetic capacity and ecological significance of marine bacterial genus Pseudoalteromonas. Mar Drugs. 2007;5(4):220–41.View ArticlePubMedPubMed CentralGoogle Scholar
  9. Suttle CA. Marine viruses - major players in the global ecosystem. Nat Rev Microbiol. 2007;5(10):801–12.View ArticlePubMedGoogle Scholar
  10. Wichels A, Biel SS, Gelderblom HR, Brinkhoff T, Muyzer G, Schütt C. Bacteriophage diversity in the North Sea. J Appl Environ Microbiol. 1998;64:4128–33.Google Scholar
  11. Duhaime MB, Wichels A, Waldmann J, Teeling H, Glöckner FO. Ecogenomics and genome landscapes of marine Pseudoalteromonas phage H105/1. ISME J. 2011;5:107–21.View ArticlePubMedGoogle Scholar
  12. Kang I, Oh HM, Kang D, Cho JC. Genome of a SAR116 bacteriophage shows the prevalence of this phage type in the oceans. Proc Natl Acad Sci U S A. 2013;110(30):12343–8.View ArticlePubMedPubMed CentralGoogle Scholar
  13. Zhao Y, Temperton B, Thrash JC, Schwalbach MS, Vergin KL, Landry ZC, et al. Abundant SAR11 viruses in the ocean. Nature. 2013;494(7437):357–60.View ArticlePubMedGoogle Scholar
  14. Krupovic M, Prangishvili D, Hendrix RW, Bamford DH. Genomics of bacterial and archaeal viruses: dynamics within the prokaryotic virosphere. Microbiol Molec Biol Rev. 2011;75(4):610–35.View ArticleGoogle Scholar
  15. Pope WH, Jacobs-Sera D, Russell DA, Peebles CL, Al-Atrache Z, Alcoser TA, et al. Expanding the diversity of mycobacteriophages: insights into genome architecture and evolution. PLoS One. 2011;6(1):e16329.View ArticlePubMedPubMed CentralGoogle Scholar
  16. Ceyssens PJ, Glonti T, Kropinski NM, Lavigne R, Chanishvili N, Kulakov L, et al. Phenotypic and genotypic variations within a single bacteriophage species. Virol J. 2011;8:134.View ArticlePubMedPubMed CentralGoogle Scholar
  17. Moebus K, Nattkemper H. Bacteriophage sensitivity patterns among bacteria isolated from marine waters. Helgol Meeresunters. 1981;34:375–85.View ArticleGoogle Scholar
  18. Flynn R, Hunkeler D, Guerin C, Burn C, Rossi P, Aragno M. Geochemical influences on H40/1 bacteriophage inactivation in glaciofluvial sands. Environ Geol. 2004;45:504–17.View ArticleGoogle Scholar
  19. Rossi P, Dorfliger N, Kennedy K, Muller I, Aragno M. Bacteriophages as surface and ground water tracers. Hydrol Earth Sys Sci. 1998;2(1):101–10.View ArticleGoogle Scholar
  20. Goldscheider G, Haller L, Poté J, Wildi W, Zopfi J. Characterizing water circulation and contaminant transport in Lake Geneva using bacteriophage tracer experiments and limnological methods. Environ Sci Technol. 2007;41(15):5252–8.View ArticlePubMedGoogle Scholar
  21. Ghanem N, Kiesel B, Kallies R, Harms H, Chatzinotas A, Wick LY. Marine phages as tracers: effects of size, morphology and physico-chemical surface properties on transport in a porous medium. Environ Sci Technol. 2016. accepted for publication.Google Scholar
  22. Kropinski AM, Prangishvili D, Lavigne R. Position paper: The creation of a rational scheme for the nomenclature of viruses of Bacteria and Archaea. Environ Microbiol. 2009;11(11):2775–7.View ArticlePubMedGoogle Scholar
  23. King AMQ, Adams MJ, Carstens EB, Lefkowitz EJ. Virus taxonomy: classification and nomenclature of viruses: Ninth Report of the International Committee on Taxonomy of Viruses. San Diego: Elsevier Academic Press; 2012.Google Scholar
  24. Qin J, Sun X, Liu Y, Berthold T, Harms H, Wick LY. Electrokinetic control of bacterial deposition and transport. Environ Sci Technol. 2015;49(9):5663–71.View ArticlePubMedGoogle Scholar
  25. Nam YD, Chang HW, Park JR, Kwon HY, Quan ZX, Park YH, et al. Pseudoalteromonas marina sp. nov., a marine bacterium isolated from tidal flats of the Yellow Sea, and reclassification of Pseudoalteromonas sagamiensis as Algicola sagamiensis comb. nov. Int J Syst Evol Microbiol. 2007;57:12–8.View ArticlePubMedGoogle Scholar
  26. Rahn O. New principles for the classification of bacteria. Zentralbl Bakteriol Parasitenkd Infektionskr Hyg Abt II. 1937;96:273.Google Scholar
  27. Skerman VBD, McGowan V, Sneath PHA. Approved Lists of Bacterial Names. Int J Syst Bacteriol. 1980;30:225.View ArticleGoogle Scholar
  28. Hurwitz BL, Sullivan MB. The Pacific Ocean Virome (POV): a marine viral metagenomic dataset and associated protein clusters for quantitative viral ecology. PLoS One. 2013;8:e57355.View ArticlePubMedPubMed CentralGoogle Scholar
  29. Küsel K, Totsche KU, Trumbore SE, Lehmann R, Steinhäuser C, Herrmann M. How Deep can surface signals be traced in the critical zone? Merging biodiversity with biogeochemistry research in a central German Muschelkalk landscape. Front Earth Sci. 2016;4:32. doi:10.3389/feart.2016.00032.View ArticleGoogle Scholar
  30. Oppenheimer CH, ZoBell CE. The growth and viability of sixty-three species of marine bacteria as influenced by hydrostatic pressure. J Mar Res. 1952;11:10–8.Google Scholar
  31. Thurber RV, Haynes M, Breitbart M, Wegley L, Rohwer F. Laboratory procedures to generate viral metagenomes. Nat Protoc. 2009;4(4):470–83. doi:10.1038/nprot.2009.10.View ArticlePubMedGoogle Scholar
  32. Lonardi S, Mirebrahim H, Wanamaker S, Alpert M, Ciardo G, Duma D, Close TJ. When less is more: 'slicing' sequencing data improves read decoding accuracy and de novo assembly quality. Bioinformatics. 2015;31(18):2972–80.View ArticlePubMedGoogle Scholar
  33. Overbeek R, Olson R, Pusch GD, Olsen GJ, Davis JJ, Disz T, et al. The SEED and the Rapid Annotation of microbial genomes using Subsystems Technology (RAST). Nucleic Acids Res. 2014;42(Database issue):D206–14. doi:10.1093/nar/gkt1226.View ArticlePubMedGoogle Scholar
  34. Delcher AL, Bratke KA, Powers EC, Salzberg SL. Identifying bacterial genes and endosymbiont DNA with Glimmer. Bioinformatics. 2007;23(6):673–9.View ArticlePubMedPubMed CentralGoogle Scholar
  35. Besemer J, Borodovsky M. GeneMark: web software for gene finding in prokaryotes, eukaryotes and viruses. Nucleic Acids Res. 2005;33:451–4.View ArticleGoogle Scholar
  36. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol. 1990;215(3):403–10.View ArticlePubMedGoogle Scholar
  37. Marchler-Bauer A, Derbyshire MK, Gonzales NR, Lu S, Chitsaz F, Geer LY, et al. CDD: NCBI's conserved domain database. Nucleic Acids Res. 2015;43(Database issue):D222–6. doi:10.1093/nar/gku1221.View ArticlePubMedGoogle Scholar
  38. Finn RD, Clements J, Arndt W, Miller BL, Wheeler TJ, Schreiber F, et al. HMMER web server: 2015 update. Nucleic Acids Res. 2015;43(W1):W30–8. doi:10.1093/nar/gkv397.View ArticlePubMedPubMed CentralGoogle Scholar
  39. Tatusov RL, Galperin MY, Natale DA, Koonin EV. The COG database: a tool for genome-scale analysis of protein functions and evolution. Nucleic Acids Res. 2000;28(1):33–6.View ArticlePubMedPubMed CentralGoogle Scholar
  40. Punta M, Coggill PC, Eberhardt RY, Mistry J, Tate J, Boursnell C. The Pfam protein families database. Nucleic Acids Res. 2012;40(Database issue):D290–301. doi:10.1093/nar/gkr1065.View ArticlePubMedGoogle Scholar
  41. Haft DH, Selengut JD, Richter RA, Harkins D, Basu MK, Beck E. TIGRFAMs and Genome Properties in 2013. Nucleic Acids Res. 2013;41(Database issue):D387–95. doi:10.1093/nar/gks1234.View ArticlePubMedGoogle Scholar
  42. Kanehisa M, Sato Y, Kawashima M, Furumichi M, Tanabe M. KEGG as a reference resource for gene and protein annotation. Nucleic Acids Res. 2016;44(D1):D457–62. doi:10.1093/nar/gkv1070.View ArticlePubMedGoogle Scholar
  43. Käll L, Krogh A, Sonnhammer EL. A combined transmembrane topology and signal peptide prediction method. J Mol Biol. 2004;338(5):1027–36.View ArticlePubMedGoogle Scholar
  44. Sullivan MJ, Petty NK, Beatson SA. Easyfig: a genome comparison visualizer. Bioinformatics. 2011;27(7):1009–10. doi:10.1093/bioinformatics/btr039.View ArticlePubMedPubMed CentralGoogle Scholar
  45. Guindon S, Gascuel O. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol. 2003;52(5):696–704.View ArticlePubMedGoogle Scholar
  46. Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, et al. Gene ontology tool for the unification of biology. Nat Genet. 2000;25:25–9.View ArticlePubMedPubMed CentralGoogle Scholar


© The Author(s). 2017